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Biology of Reproduction 60, 277-282 (1999)
©Copyright 1999 Society for the Study of Reproduction, Inc.

Noradrenaline Stimulates the Production of Prostaglandin F2{alpha} in Cultured Bovine Endometrial Cells1

Dariusz J Skarzynskia,b, Yoshihisa Uenoyamaa, Jan Kotwicab, and Kiyoshi Okuda2,a

a Laboratory of Reproductive Endocrinology, Faculty of Agriculture, Okayama University, Okayama 700-8530, Japan b Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10-718 Olsztyn-Kortowo, Poland


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The stimulatory effect of noradrenaline (NA) as well as oxytocin (OT) on bovine endometrial prostaglandin (PG) F2{alpha} production, and the intracellular mechanisms of their actions, were investigated in cultured bovine endometrial cells (a mixture of epithelial, stromal, and glandular cells). The cells were cultured in Dulbecco's Modified Eagle's medium and Ham's F-12 medium (1:1 [v:v]) with 10% calf serum. When the cells reached confluence, the culture medium was replaced with fresh medium with 0.1% BSA and various doses of NA (10-8–10-4 M). NA stimulated PGF2{alpha} production in a dose-dependent manner (p < 0.05). To evaluate the intracellular mechanisms of NA and OT actions, the cells were treated with forskolin (an activator of adenylate cyclase), phorbol 12-myristate 13-acetate (PMA, an activator of protein kinase [PK] C), Rp-cAMP (a competitive cAMP antagonist and an inhibitor of PKA), U-73122 (an inhibitor of phospholipase [PL] C), or anthranilic acid (ACA, an inhibitor of PLA2). Forskolin and PMA stimulated PGF2{alpha} production in a dose-dependent manner (p < 0.05). Rp-cAMP completely inhibited (p < 0.001) the NA-induced, but not the OT-induced, PGF2{alpha} production. Although U-73122 inhibited only OT-induced PGF2{alpha} production (p < 0.001), ACA completely stopped the actions of NA and OT. The overall results indicate that NA as well as OT is involved in the regulation of the endometrial PGF2{alpha} production in cattle and that the stimulatory effects of NA and OT on PGF2{alpha} production are mediated via the PKA and PKC pathways, respectively.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The role of uterine prostaglandin (PG) F2{alpha} in the demise of the corpus luteum at the end of the estrous cycle is well established in ruminants (reviewed by Poyser [1]). It is generally accepted that ovarian oxytocin (OT) and its uterine receptors take part in the initiation of luteolysis [2, 3]. Although immunization against OT and administration of an OT antagonist block luteolysis in sheep and goats [4–6], the blockade of uterine OT receptors with a specific OT antagonist from Day 15 until Day 22 of the cycle affects neither luteolysis nor the duration of the estrous cycle compared with values in control heifers [7]. Therefore, we hypothesize that PGF2{alpha} production from the bovine endometrium is regulated by not only OT but also one or more other factors that initiate PGF2{alpha} release.

The effects of sympathetic nerve stimulation and of the administration of catecholamines on the output of prostaglandins from several tissues have been widely studied. There is general agreement that adrenergic stimuli increase the synthesis of prostaglandins [8, 9]. However, contradictory results regarding catecholamine-stimulated PGF2{alpha} production from the uterus have also been reported: noradrenaline (NA) depressed the output of PGF2{alpha} from isolated rat uterus [10] and sow oviducts [11]. On the other hand, catecholamines have been found to stimulate PGF2{alpha} production in the rat [12] and human [13] uterus.

Adrenergic receptors are believed to induce cellular responses by increasing the activity of membrane-bound regulatory proteins that bind G proteins [14, 15]. ß-Adrenergic receptors activate the plasma membrane enzyme adenylate cyclase, leading to the generation of cAMP and activation of protein kinase (PK) A. In contrast, {alpha}-adrenergic receptors are coupled to processes that lead to changes in phosphatidylinositol turnover and finally to the activation of PKC and the mobilization of intracellular Ca2+. Moreover, the synthesis of prostaglandins is associated with an increase in the activity of phospholipase (PL) A2 in many cell types [16]. It has been suggested that two intracellular mechanisms, PLC and PLA2, mediate the stimulatory effect of OT on the release of PGF2{alpha} from ovine [17] and bovine [18] endometrial tissues.

In the present study, to examine the hypothesis that PGF2{alpha} production from the bovine endometrium depends on not only OT but also other factor(s), we investigated the stimulatory effect of NA as well as OT on PGF2{alpha} production from bovine endometrial cells through use of a cell culture system. The intracellular mechanisms of their actions were also studied.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Isolation of Endometrial Cells

Bovine uteri were obtained from a local abattoir and placed on ice until further processing at the laboratory. The stage of the estrous cycle was estimated by macroscopic observation of the ovary [19, 20]. The recovery of endometrial cells and their viability after isolation were optimal in the early luteal stage (Days 2–4 after ovulation) of the estrous cycle as reported previously [21, 22]. Accordingly, only tissues assigned to this stage of the estrous cycle were used in this study. Cells were isolated as described by Freidman et al. [23] with some modifications. Briefly, uteri were washed in sterile, Ca2+- and Mg2+-free Hanks' Balanced Salt solution (HBSS) with penicillin (100 IU/ml) and streptomycin (100 µg/ml). The uterine horn ipsilateral to the corpus luteum was cut transversely with scissors into several segments, which were slit to expose the endometrial surface. The endometrial strips were dissected from the myometrial layer with a scalpel and then washed three times in 50 ml of sterile HBSS containing antibiotics. The endometrial strips were then minced into small pieces (1 mm3). The minced tissues (approximately 5 g) were stirred in 50 ml of HBSS with 0.05% collagenase I (Sigma Chemical Co., St. Louis, MO; #C-0130) and 0.1% BSA (Boehringer Mannheim GmbH, Mannheim, Germany; #735078). After 15-min stirring, the solution was discarded to remove mechanically decomposed endometrial cells. The tissues were then digested twice at 37°C for 45 min in 50 ml of the sterile HBSS containing 0.05% collagenase I, 0.005% DNase I (Sigma; #D-1152), and 0.1% BSA. Dissociated cells were filtered through metal meshes (150 µm and 80 µm) to remove undissociated tissue fragments. The filtrates obtained from the first and second digestions were mixed. The cells were washed three times by centrifugation for 10 min at 150 x g with Dulbecco's Modified Eagle's medium (DMEM; Sigma; #D-1152). After three washes, the cells were counted with a hemocytometer. The obtained cells consisted of epithelial, stromal, and glandular cells. The cell viability was higher than 80% as assessed by 0.5% trypan blue dye exclusion.

Culture of Endometrial Cells

The final pellets were resuspended in culture medium (DMEM/Ham's F-12, 1:1 [v:v]; Sigma; #D-8900) supplemented with 10% calf serum (Sigma; #C-6278) and 20 µg/ml gentamicin. The cells were seeded at a density of 1 x 105 viable cells/ml in 48-well plates (Costar, Cambridge, MA) and cultured at 37.5°C in a humidified atmosphere of 5% CO2 in air. The culture medium was changed every 2 days until the cells reached confluence 5 or 6 days after the start of culture. When the cells were confluent, the medium was replaced with fresh DMEM/Ham's F-12 supplemented with 0.1% BSA. The cells were then exposed to various stimulators for the following experiments.

Experiment 1

To establish the most effective dose and exposure time of NA, the bovine endometrial cells were incubated with various concentrations of NA (10-8–10-4 M; Sigma; #A-9512) and OT (10-7 M; kindly donated by Teikoku Hormone MFG Co., Tokyo, Japan). Conditioned media were collected after 2, 4, and 6 h of incubations.

Experiment 2

To determine the receptor type mediating the response to NA, the endometrial cells were incubated with propranolol (PROP; a nonselective ß-adrenergic antagonist; Sigma; #P-0884; 10-5 M) or phentolamine (PHEN; a nonselective {alpha}-adrenergic antagonist; Sigma; #P-7547; 10-5 M) with NA (10-5 M) for 4 h.

Experiment 3

To determine the subtypes of ß-adrenergic receptors mediating the NA-stimulated PGF2{alpha} production, the endometrial cells were incubated with a nonselective ß-adrenergic agonist (isoproterenol; RBI, Natick, MA; #70–0811–04; 10-5 M), a selective ß1-adrenergic agonist (dobutamine; RBI; #70–0301–72; 10-5 M), a selective ß2-adrenergic receptor agonist (salbutamol; Sigma; #S5013; 10-5 M), or a selective ß3-adrenergic agonist (BRL 37344 sodium; RBI; #70–0101–69; 10-5 M) for the final 4 h of culture.

Experiment 4

The effects of forskolin (an adenylate cyclase activator; RBI; #F-105) and phorbol 12-myristate 13-acetate (PMA; a PKC activator; Sigma; #P-8139) on the release of PGF2{alpha} were examined. When the endometrial cells reached confluence, the cells were exposed to forskolin (10-10–10-5 M), PMA (10-10–10-5 M), NA (10-5 M), or OT (10-7 M) for the final 4 h of culture.

Experiment 5

To determine the intracellular mechanisms of NA as well as OT actions on the endometrial cells, the cells were exposed to a competitive cAMP antagonist and PKA inhibitor (Rp-cAMP; RBI; #A-165S; 10-5 M), a PLC inhibitor (U-73122; Calbiochem, San Diego, CA; #662035; 10-5 M), or a PLA2 inhibitor (anthranilic acid, ACA; Calbiochem; #104550; 10-5 M) with NA (10-5 M) or OT (10-7 M) for 4 h.

At the end of each experiment, the culture media were stored at -30°C until the PGF2{alpha} assay. The DNA content was estimated by a spectrophotometric method as described by Labarca and Paigen [24]. DNA contents were used to estimate the number of cells in each well and to standardize the results. Cell numbers were estimated mathematically using 1.4 x 105 cells/µg DNA as a conversion factor.

Hormone Determination

Concentrations of PGF2{alpha} were determined directly in the media with an enzyme immunoassay technique described previously [25] using peroxidase-labeled PGF2{alpha} as a tracer (1:10 000) and anti-PGF2{alpha} serum (1:40 000 final dilution; donated by Dr. Seiji Ito of Kansai Medical University, Osaka, Japan). The PGF2{alpha} standard curve ranged from 15.625 pg/ml to 4000 pg/ml, and the ED50 of the assay was 250 pg/ml. The intra- and interassay coefficients of variation were 7.4% (n = 10) and 11.6% (n = 10), respectively.

Statistical Analysis

The data are shown as the mean ± SEM of values obtained in 3–4 separate experiments, each performed in triplicate. The statistical significance of differences between controls and treated groups was assessed by one-way ANOVA followed by Bonferroni's multiple comparison test (GraphPad PRISM; GraphPad Software, Inc., San Diego, CA).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Acute Effects of NA and OT on PGF2{alpha} Production

PGF2{alpha} production from the cells increased (p < 0.01) to 2- to 3-fold compared to controls in response to NA and OT at all three exposure times (Fig. 1). The highest stimulation (290%; p < 0.001) was observed when the cells were incubated with 10-5 M NA for 4 h.



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  		FIG. 1. Effects of NA and OT on PGF2{alpha} production by cultured bovine endometrial cells (mean ± SEM, n = 3). NA (10-8–10-4 M) or OT (10-7 M) was added at 2, 4, or 6 h before the end of culture. Different superscript letters indicate significant differences (p < 0.05 or lower) as determined by ANOVA followed by Bonferroni's multiple comparison test.

Effects of {alpha}- and ß-Adrenergic Receptor Blockers on NA-Stimulated PGF2{alpha} Production

PHEN ({alpha}-adrenergic antagonist; 10-5 M) had no effect on basal PGF2{alpha} production (Fig. 2) and did not inhibit the NA-stimulated release of PGF2{alpha} (p > 0.05). However, PROP (ß-adrenergic antagonist; 10-5 M) suppressed (p < 0.001) the NA-induced increase in PGF2{alpha} production (Fig. 2), although PROP had no effect on PGF2{alpha} concentrations when administered alone (p > 0.05).



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  		FIG. 2. Effects of PROP (a nonselective ß-adrenergic antagonist; 10-5 M) and PHEN (a nonselective {alpha}-adrenergic antagonist; 10-5 M) on NA (10-5 M)-stimulated PGF2{alpha} production by bovine endometrial cells (mean ± SEM, n = 4). NA, PROP, and PHEN were added 4 h before the end of culture. Different superscript letters indicate significant differences (p < 0.001) as determined by ANOVA followed by Bonferroni's multiple comparison test.

PGF2{alpha} Production in Response to the Various ß-Adrenergic Agonists

Isoproterenol (a nonselective ß-adrenergic agonist; 10-5 M) and salbutamol (a selective ß2-adrenergic agonist; 10-5 M) stimulated PGF2{alpha} production (p < 0.001; Table 1) above the basal level to 414% and 470%, respectively. PGF2{alpha} production from the cells also increased (p < 0.05 or lower) by 2- to 3-fold in response to dobutamine (a ß1-adrenergic agonist; 10-5 M) and BRL 37344 (a selective ß3-adrenergic agonist; 10-5 M). Moreover, NA (10-5 M) significantly increased PGF2{alpha} production (p < 0.05; Table 1), but the effect of NA was less potent than that of salbutamol (p < 0.05).


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  		TABLE 1. Effects of OT, NA, and ß-adrenergic agonists on PGF2{alpha} production by cultured bovine endometrial cells (mean ± SEM, n = 3).

Second Messenger Systems in the Stimulation of PGF2{alpha} Production

Both forskolin (10-10–10-5 M) and PMA (10-10-10-5 M) stimulated PGF2{alpha} production in a dose-dependent manner (p < 0.05 or lower; Fig. 3, a and b). The highest stimulation with forskolin was observed at a concentration of 10-8 M (by 242%; p < 0.001). PMA (10-8 M) showed a more potent effect on the production of PGF2{alpha} (605%; p < 0.0001) than did forskolin, NA, and OT.



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  		FIG. 3. Effects of a) forskolin (an adenylate cyclase activator) and b) PMA (a PKC activator) on PGF2{alpha} production by bovine endometrial cells (mean ± SEM, n = 4). Forskolin (10-10–10-5 M), PMA (10-10–10-5 M), NA (10-5 M), or OT (10-7 M) was added 4 h before the end of culture. Different superscript letters indicate significant differences (p < 0.05 or lower) as determined by ANOVA followed by Bonferroni's multiple comparison test.

Intracellular Mechanisms of NA and OT Actions

Rp-cAMP (a PKA inhibitor) completely inhibited (p < 0.001) the stimulatory effect of NA on PGF2{alpha} production (Fig. 4a), but U-73122 (a PLC inhibitor) stopped only OT-induced PGF2{alpha} production (p < 0.001; Fig. 4b). However, ACA (a PLA2 inhibitor) completely suppressed the actions of NA and OT.



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  		FIG. 4. Effects of PLA2 inhibitor (ACA), PKA inhibitor (Rp-cAMP), and PLC inhibitor (U-73122) on a) NA- and b) OT-stimulated PGF2{alpha} production by bovine endometrial cells (mean ± SEM, n = 4). ACA (10-5 M), Rp-cAMP (10-5 M), U-73122 (10-5 M), NA (10-5 M), and OT (10-7 M) were added 4 h before the end of culture. Different superscript letters indicate significant differences (p < 0.001) as determined by ANOVA followed by Bonferroni's multiple comparison test.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study demonstrated for the first time that NA stimulates PGF2{alpha} production by cultured bovine endometrial cells. These cultured cells were composed of epithelial, stromal, and glandular cells. The cells have been well characterized by morphological and functional properties [21]. Since PGF2{alpha} is produced mainly by epithelial cells, it may be assumed that stimulation of PGF2{alpha} production by NA also occurs in the epithelial cells. However, the localization of ß-adrenergic receptors in bovine endometrial tissue has not been defined. Further studies are needed to clarify the target cells of NA. The stimulatory effects were observed at concentrations between 10-8 and 10-4 M. It has been well demonstrated that bovine reproductive organs such as the ovary and uterus produce large amounts of catecholamines [26–29]. Therefore, although the NA concentrations applied in the present study were relatively high compared with those in blood plasma (2 x 10-9 M) [30], we assume that endogenous NA may locally have an enhancing effect on PGF2{alpha} production in the bovine endometrium.

The effect of NA on endometrial PGF2{alpha} production was completely inhibited by treatment with 10-5 M PROP (a nonselective ß-adrenergic antagonist) in the present study. This result clearly demonstrated that the response of bovine endometrial cells to NA stimulation is mediated through ß-adrenergic receptors (Fig. 2). It has been clearly shown that PROP suppresses the basal release of PGF2{alpha} in the rat uterus [12]. ß-Adrenergic receptors were detected in rat uterus [31] and in guinea pig [32] and bovine [33] myometrium. The concentrations of NA (10-8–10-4 M) that increased PGF2{alpha} production in the present study are compatible with the affinity of ß-adrenergic receptors in rat endometrium reported previously (Kd = 1.5 x 10-8 M; [31]). Moreover, all the adrenergic agonists that were used in the present study stimulated PGF2{alpha} production (Table 1). In view of the above findings, we postulate that the stimulatory effect of NA on PGF2{alpha} production is mediated by ß-adrenergic receptors, possibly by ß2-adrenergic receptors, in bovine endometrial cells.

It is commonly believed that ß-adrenergic receptors activate adenylate cyclase, cAMP-dependent PK, and phosphorylation of crucial cellular substrates that lead to physiological effects [14]. The stimulation of PGF2{alpha} release from bovine endometrial cells by forskolin implies that cAMP and PKA play important roles in regulating the endometrial release of PGF2{alpha}. We assume, therefore, that PKA might mediate the stimulatory effect of NA on PGF2{alpha} production. This supposition that the cAMP-PKA pathway is important in NA-stimulated PGF2{alpha} production by bovine endometrial cells is supported by the results of our final experiments (Fig. 4). Rp-cAMP (a PKA inhibitor) completely inhibited NA-induced, but not OT-induced, PGF2{alpha} production. Furthermore, U-73122 (a PLC inhibitor) suppressed only the PGF2{alpha} production stimulated by OT. These results suggest that the stimulatory effects of NA and OT on PGF2{alpha} production may be mediated via separate signaling pathways: NA affects PGF2{alpha} production via the cAMP-PKA pathway. In contrast, the action of OT may be mediated by the PLC-PKC pathway.

It has been clearly demonstrated that an increase in PLA2 activity is associated with PGF2{alpha} production from the uterus in many species [1, 18, 34]. Indeed, the stimulatory actions of both OT and NA were completely reduced by ACA (a PLA2 inhibitor) in the present study. These findings suggest that both PKC and PKA may affect PLA2 activity. It is well known that the activation of PLA2 is induced by increases of intracellular calcium concentration and of PKC activity [35]. In contrast, the interaction between PKA and PLA2 is not well understood. On the other hand, it is well established that PLA2 stimulates intracellular arachidonic acid accumulation. Therefore, the failure of NA and OT to stimulate PGF2{alpha} production in endometrial cells treated with ACA (a PLA2 inhibitor) might be due to a lower accumulation of arachidonic acid, as a precursor of PGF2{alpha}, in the cells.

Our results clearly demonstrated that NA and the stimulation of ß-adrenergic receptors enhance PGF2{alpha} production from cultured bovine endometrial cells. Moreover, we recently demonstrated the possible actions of NA on endometrial PGF2{alpha} output in heifers during luteolysis [36]. These findings support our hypothesis that PGF2{alpha} production is regulated by not only OT but also one or more factors, and suggest that NA plays an important role as one of the regulators of endometrial PGF2{alpha} production. However, since only tissues assigned to early luteal stage were used in the present study and the cells were cultured in serum-supplemented medium for 5–6 days, the cells might not show the function of early stage or that of luteolysis. Additionally, the localization and cyclic changes of the ß-adrenergic receptors and the correlation between OT and NA on PGF2{alpha} production have not been defined in bovine endometrium as well as they have been in myometrium. Besides PGF2{alpha} production, NA seems to have inhibitory and excitatory effects on uterine contraction and blood flow in vivo through the activation of ß- and {alpha}-adrenergic receptors, respectively [37]. Furthermore, the switch from {alpha}- to ß-receptor-mediated response appears to be regulated by ovarian hormones [38, 39]. Further in vivo and in vitro studies are needed to clarify these points.

In conclusion, the present study postulated that NA as well as OT is involved in the regulation of endometrial PGF2{alpha} production in cattle, and that NA action is mediated by ß-adrenergic receptors and the cAMP-PKA pathway whereas OT acts through the PLC-PKA pathway.


   ACKNOWLEDGMENTS
 
The authors thank Dr. Heinrich Meyer of Technical University of Munich for peroxidase-labeled PGF2{alpha}, Dr. Seiji Ito of Kansai Medical College for the anti-PGF2{alpha} serum, and Teikoku Hormone MFG. Co., Tokyo, Japan, for generously providing synthetic oxytocin.


   FOOTNOTES
 
1 This research was supported by the Polish National Research Council (KBN 5 P06K 027 13), Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan (No. 96346), the Japanese-German Cooperative Science Promotion Program of the Japanese Society for the Promotion of Science (JSPS), and a grant for the specific research "The study of the development of organisms effective to environmental conservation for human life" at Okayama University in 1998–1999. D.J.S. is a postdoctoral fellow supported by JSPS. Back

2 Correspondence. FAX: 81 86 251 8388; kokuda{at}cc.okayama-u.ac.jp Back

Accepted: September 9, 1998.

Received: May 4, 1998.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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